Distinct roles of P2X receptors in modulating glutamate release at different primary sensory synapses in rat spinal cord

被引:77
作者
Nakatsuka, T [1 ]
Tsuzuki, K [1 ]
Ling, JX [1 ]
Sonobe, H [1 ]
Gu, JGG [1 ]
机构
[1] Univ Florida, Coll Dent, Dept Oral Surg, Div Neurosci,McKnight Brain Inst, Gainesville, FL 32610 USA
关键词
D O I
10.1152/jn.01172.2002
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Using spinal cord slice preparations and patch-clamp recordings in lamina II and lamina V regions, we tested a hypothesis that P2X receptor subtypes differentially modulate glutamate release from primary afferent terminals innervating different sensory regions. We found that activation of P2X receptors by alpha,beta-methylene-ATP increased glutamate release onto >80% of DH neurons in both lamina regions. However, two distinct types of modulation, a transient and a long-lasting enhancement of glutamate release were observed. In lamina II recordings, >70% of the modulation was transient. In contrast, P2X receptor-mediated modulation was always long-lasting in lamina V. Pharmacologically, both transient and long-lasting types of modulation were blocked by 10 muM pyridxal-phospahte-6-azophenyl-2',4'-disulphonic acid tetrasodium, a broad-spectrum P2X receptor antagonist. Transient modulation was not observed in the presence of 1 muM trinitrophenyl-ATP (TNP-ATP), a subtype-selective P2X receptor antagonist, suggesting that homomeric P2X(3) receptors may be involved in the transient modulation in lamina II. The long-lasting modulation remained in the presence of 1 muM TNP-ATP. Selective removal of P2X(3)-expressing afferent terminals by the targeting toxin saporin-conjugated isolectin B4 or surgical removal of superficial DH did not affect P2X receptor-mediated long-lasting modulation in lamina V. Taken together, these results suggest that P2X receptor subtypes play distinct roles in sensory processing in functionally different sensory regions.
引用
收藏
页码:3243 / 3252
页数:10
相关论文
共 54 条
  • [41] Evidence for the involvement of spinal endogenous ATP and P2X receptors in nociceptive responses caused by formalin and capsaicin in mice
    Tsuda, M
    Ueno, S
    Inoue, K
    [J]. BRITISH JOURNAL OF PHARMACOLOGY, 1999, 128 (07) : 1497 - 1504
  • [42] In vivo pathway of thermal hyperalgesia by intrathecal administration of α,β-methylene ATP in mouse spinal cord:: Involvement of the glutamate-NMDA receptor system
    Tsuda, M
    Ueno, S
    Inoue, K
    [J]. BRITISH JOURNAL OF PHARMACOLOGY, 1999, 127 (02) : 449 - 456
  • [43] Mechanical allodynia caused by intraplantar injection of P2X receptor agonist in rats:: Involvement of heteromeric P2X2/3 receptor signaling in capsaicin-insensitive primary afferent neurons
    Tsuda, M
    Koizumi, S
    Kita, A
    Shigemoto, Y
    Ueno, S
    Inoue, K
    [J]. JOURNAL OF NEUROSCIENCE, 2000, 20 (15)
  • [44] TNP-ATP-resistant P2X ionic current on the central terminals and somata of rat primary sensory neurons
    Tsuzuki, K
    Ase, A
    Séguéla, P
    Nakatsuka, T
    Wang, CY
    She, JX
    Gu, JGG
    [J]. JOURNAL OF NEUROPHYSIOLOGY, 2003, 89 (06) : 3235 - 3242
  • [45] Cell type-specific ATP-activated responses in rat dorsal root ganglion neurons
    Ueno, S
    Tsuda, M
    Iwanaga, T
    Inoue, K
    [J]. BRITISH JOURNAL OF PHARMACOLOGY, 1999, 126 (02) : 429 - 436
  • [46] NEW CLASS OF LIGAND-GATED ION-CHANNEL DEFINED BY P-2X RECEPTOR FOR EXTRACELLULAR ATP
    VALERA, S
    HUSSY, N
    EVANS, RJ
    ADAMI, N
    NORTH, RA
    SURPRENANT, A
    BUELL, G
    [J]. NATURE, 1994, 371 (6497) : 516 - 519
  • [47] Virginio C, 1998, MOL PHARMACOL, V53, P969
  • [48] Cytotoxic targeting of isolectin IB4-binding sensory neurons
    Vulchanova, L
    Olson, TH
    Stone, LS
    Riedl, MS
    Elde, R
    Honda, CN
    [J]. NEUROSCIENCE, 2001, 108 (01) : 143 - 155
  • [49] P2X3 is expressed by DRG neurons that terminate in inner lamina II
    Vulchanova, L
    Riedl, MS
    Shuster, SJ
    Stone, LS
    Hargreaves, KM
    Buell, G
    Surprenant, A
    North, RA
    Elde, R
    [J]. EUROPEAN JOURNAL OF NEUROSCIENCE, 1998, 10 (11) : 3470 - 3478
  • [50] Immunohistochemical study of the P2X(2) and P2X(3) receptor subunits in rat and monkey sensory neurons and their central terminals
    Vulchanova, L
    Riedl, MS
    Shuster, SJ
    Buell, G
    Surprenant, A
    North, RA
    Elde, R
    [J]. NEUROPHARMACOLOGY, 1997, 36 (09) : 1229 - 1242